IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-46082-5.html
   My bibliography  Save this article

Interplay between coding and non-coding regulation drives the Arabidopsis seed-to-seedling transition

Author

Listed:
  • Benjamin J. M. Tremblay

    (Centre for Research in Agricultural Genomics (CRAG), CSIC-IRTA-UAB-UB, Campus UAB, Bellaterra)

  • Cristina P. Santini

    (Centre for Research in Agricultural Genomics (CRAG), CSIC-IRTA-UAB-UB, Campus UAB, Bellaterra)

  • Yajiao Cheng

    (Centre for Research in Agricultural Genomics (CRAG), CSIC-IRTA-UAB-UB, Campus UAB, Bellaterra)

  • Xue Zhang

    (Swedish University of Agricultural Sciences (SLU))

  • Stefanie Rosa

    (Swedish University of Agricultural Sciences (SLU))

  • Julia I. Qüesta

    (Centre for Research in Agricultural Genomics (CRAG), CSIC-IRTA-UAB-UB, Campus UAB, Bellaterra)

Abstract

Translation of seed stored mRNAs is essential to trigger germination. However, when RNAPII re-engages RNA synthesis during the seed-to-seedling transition has remained in question. Combining csRNA-seq, ATAC-seq and smFISH in Arabidopsis thaliana we demonstrate that active transcription initiation is detectable during the entire germination process. Features of non-coding regulation such as dynamic changes in chromatin accessible regions, antisense transcription, as well as bidirectional non-coding promoters are widespread throughout the Arabidopsis genome. We show that sensitivity to exogenous ABSCISIC ACID (ABA) during germination depends on proximal promoter accessibility at ABA-responsive genes. Moreover, we provide genetic validation of the existence of divergent transcription in plants. Our results reveal that active enhancer elements are transcribed producing non-coding enhancer RNAs (eRNAs) as widely documented in metazoans. In sum, this study defining the extent and role of coding and non-coding transcription during key stages of germination expands our understanding of transcriptional mechanisms underlying plant developmental transitions.

Suggested Citation

  • Benjamin J. M. Tremblay & Cristina P. Santini & Yajiao Cheng & Xue Zhang & Stefanie Rosa & Julia I. Qüesta, 2024. "Interplay between coding and non-coding regulation drives the Arabidopsis seed-to-seedling transition," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46082-5
    DOI: 10.1038/s41467-024-46082-5
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-46082-5
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-46082-5?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Xinyue Zhao & Jingrui Li & Bi Lian & Hanqing Gu & Yan Li & Yijun Qi, 2018. "Global identification of Arabidopsis lncRNAs reveals the regulation of MAF4 by a natural antisense RNA," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    2. Zeileis, Achim & Grothendieck, Gabor, 2005. "zoo: S3 Infrastructure for Regular and Irregular Time Series," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 14(i06).
    3. Hiroaki Fujii & Viswanathan Chinnusamy & Americo Rodrigues & Silvia Rubio & Regina Antoni & Sang-Youl Park & Sean R. Cutler & Jen Sheen & Pedro L. Rodriguez & Jian-Kang Zhu, 2009. "In vitro reconstitution of an abscisic acid signalling pathway," Nature, Nature, vol. 462(7273), pages 660-664, December.
    4. L. Stirling Churchman & Jonathan S. Weissman, 2011. "Nascent transcript sequencing visualizes transcription at nucleotide resolution," Nature, Nature, vol. 469(7330), pages 368-373, January.
    5. Ting Zhao & Jingyun Lu & Huairen Zhang & Mande Xue & Jie Pan & Lijun Ma & Frédéric Berger & Danhua Jiang, 2022. "Histone H3.3 deposition in seed is essential for the post-embryonic developmental competence in Arabidopsis," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    6. Stefanie Rosa & Susan Duncan & Caroline Dean, 2016. "Mutually exclusive sense–antisense transcription at FLC facilitates environmentally induced gene repression," Nature Communications, Nature, vol. 7(1), pages 1-7, December.
    7. Helen Neil & Christophe Malabat & Yves d’Aubenton-Carafa & Zhenyu Xu & Lars M. Steinmetz & Alain Jacquier, 2009. "Widespread bidirectional promoters are the major source of cryptic transcripts in yeast," Nature, Nature, vol. 457(7232), pages 1038-1042, February.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Benjamin J. E. Martin & LeAnn J. Howe, 2022. "Reply to: Pitfalls in using phenanthroline to study the causal relationship between promoter nucleosome acetylation and transcription," Nature Communications, Nature, vol. 13(1), pages 1-4, December.
    2. Zhen-Hui Wang & Xin-Feng Wang & Tianyuan Lu & Ming-Rui Li & Peng Jiang & Jing Zhao & Si-Tong Liu & Xue-Qi Fu & Jonathan F. Wendel & Yves Peer & Bao Liu & Lin-Feng Li, 2022. "Reshuffling of the ancestral core-eudicot genome shaped chromatin topology and epigenetic modification in Panax," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    3. Malte Willmes & Katherine M Ransom & Levi S Lewis & Christian T Denney & Justin J G Glessner & James A Hobbs, 2018. "IsoFishR: An application for reproducible data reduction and analysis of strontium isotope ratios (87Sr/86Sr) obtained via laser-ablation MC-ICP-MS," PLOS ONE, Public Library of Science, vol. 13(9), pages 1-15, September.
    4. Bingnan Li & Patrice Zeis & Yujie Zhang & Alisa Alekseenko & Eliska Fürst & Yerma Pareja Sanchez & Gen Lin & Manu M. Tekkedil & Ilaria Piazza & Lars M. Steinmetz & Vicent Pelechano, 2023. "Differential regulation of mRNA stability modulates transcriptional memory and facilitates environmental adaptation," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    5. Michael Berlemann & Julia Freese & Sven Knoth, 2020. "Dating the start of the US house price bubble: an application of statistical process control," Empirical Economics, Springer, vol. 58(5), pages 2287-2307, May.
    6. Zhang You & Shiyuan Guo & Qiao Li & Yanjun Fang & Panpan Huang & Chuanfeng Ju & Cun Wang, 2023. "The CBL1/9-CIPK1 calcium sensor negatively regulates drought stress by phosphorylating the PYLs ABA receptor," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    7. Judith M. Ament & Robin Freeman & Chris Carbone & Anna Vassall & Charlotte Watts, 2020. "An Empirical Analysis of Synergies and Tradeoffs between Sustainable Development Goals," Sustainability, MDPI, vol. 12(20), pages 1-12, October.
    8. Percebois, Jacques & Pommeret, Stanislas, 2019. "Storage cost induced by a large substitution of nuclear by intermittent renewable energies: The French case," Energy Policy, Elsevier, vol. 135(C).
    9. Ferstl, Robert & Hayden, Josef, 2010. "Zero-Coupon Yield Curve Estimation with the Package termstrc," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 36(i01).
    10. Golyandina, Nina & Korobeynikov, Anton & Shlemov, Alex & Usevich, Konstantin, 2015. "Multivariate and 2D Extensions of Singular Spectrum Analysis with the Rssa Package," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 67(i02).
    11. Thelma Dede Baddoo & Zhijia Li & Yiqing Guan & Kenneth Rodolphe Chabi Boni & Isaac Kwesi Nooni, 2020. "Data-Driven Modeling and the Influence of Objective Function Selection on Model Performance in Limited Data Regions," IJERPH, MDPI, vol. 17(11), pages 1-26, June.
    12. Hansin Bilgili & Chwen Sheu, 2022. "A Bibliometric Review of the Mathematics Journal," Mathematics, MDPI, vol. 10(15), pages 1-17, July.
    13. Jia Zhou & Qinli Hu & Xinlong Xiao & Deqiang Yao & Shenghong Ge & Jin Ye & Haojie Li & Rujie Cai & Renyang Liu & Fangang Meng & Chao Wang & Jian-Kang Zhu & Mingguang Lei & Weiman Xing, 2021. "Mechanism of phosphate sensing and signaling revealed by rice SPX1-PHR2 complex structure," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    14. Maxime Duval & Carlo Yague-Sanz & Tomasz W. Turowski & Elisabeth Petfalski & David Tollervey & François Bachand, 2023. "The conserved RNA-binding protein Seb1 promotes cotranscriptional ribosomal RNA processing by controlling RNA polymerase I progression," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    15. Golyandina, Nina & Korobeynikov, Anton, 2014. "Basic Singular Spectrum Analysis and forecasting with R," Computational Statistics & Data Analysis, Elsevier, vol. 71(C), pages 934-954.
    16. Nikolaus Umlauf & Georg Mayr & Jakob Messner & Achim Zeileis, 2011. "Why Does It Always Rain on Me? A Spatio-Temporal Analysis of Precipitation in Austria," Working Papers 2011-25, Faculty of Economics and Statistics, Universität Innsbruck.
    17. repec:jss:jstsof:40:i03 is not listed on IDEAS
    18. Matthias Bannert, 2015. "timeseriesdb: Manage and Archive Time Series Data in Establishment Statistics with R and PostgreSQL," KOF Working papers 15-384, KOF Swiss Economic Institute, ETH Zurich.
    19. Jonathan Liu & Donald Hansen & Elizabeth Eck & Yang Joon Kim & Meghan Turner & Simon Alamos & Hernan Garcia, 2021. "Real-time single-cell characterization of the eukaryotic transcription cycle reveals correlations between RNA initiation, elongation, and cleavage," PLOS Computational Biology, Public Library of Science, vol. 17(5), pages 1-26, May.
    20. Ohana-Levi, Noa & Ben-Gal, Alon & Munitz, Sarel & Netzer, Yishai, 2022. "Grapevine crop evapotranspiration and crop coefficient forecasting using linear and non-linear multiple regression models," Agricultural Water Management, Elsevier, vol. 262(C).
    21. Raquel Martins Lana & Maíra Moreira Morais & Tiago França Melo de Lima & Tiago Garcia de Senna Carneiro & Lucas Martins Stolerman & Jefferson Pereira Caldas dos Santos & José Joaquín Carvajal Cortés &, 2018. "Assessment of a trap based Aedes aegypti surveillance program using mathematical modeling," PLOS ONE, Public Library of Science, vol. 13(1), pages 1-16, January.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46082-5. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.